A novel ATP dependent dimethylsulfoniopropionate lyase in bacteria that releases dimethyl sulfide and acryloyl-CoA

  1. Chun-Yang Li
  2. Xiu-Juan Wang
  3. Xiu-Lan Chen
  4. Qi Sheng
  5. Shan Zhang
  6. Peng Wang
  7. Mussa Quareshy
  8. Branko Rihtman
  9. Xuan Shao
  10. Chao Gao
  11. Fuchuan Li
  12. Shengying Li
  13. Weipeng Zhang
  14. Xiao-Hua Zhang
  15. Gui-Peng Yang
  16. Jonathan D Todd
  17. Yin Chen
  18. Yu-Zhong Zhang  Is a corresponding author
  1. Ocean University of China, China
  2. Shandong University, China
  3. University of Warwick, United Kingdom
  4. University of East Anglia, United Kingdom

Abstract

Dimethylsulfoniopropionate (DMSP) is an abundant and ubiquitous organosulfur molecule in marine environments with important roles in global sulfur and nutrient cycling. Diverse DMSP lyases in some algae, bacteria and fungi cleave DMSP to yield gaseous dimethyl sulfide (DMS), an infochemical with important roles in atmospheric chemistry. Here we identified a novel ATP-dependent DMSP lyase, DddX. DddX belongs to the acyl-CoA synthetase superfamily and is distinct from the eight other known DMSP lyases. DddX catalyses the conversion of DMSP to DMS via a two-step reaction: the ligation of DMSP with CoA to form the intermediate DMSP-CoA, which is then cleaved to DMS and acryloyl-CoA. The novel catalytic mechanism was elucidated by structural and biochemical analyses. DddX is found in several Alphaproteobacteria, Gammaproteobacteria and Firmicutes, suggesting that this new DMSP lyase may play an overlooked role in DMSP/DMS cycles.

Data availability

The draft genome sequences of Psychrobacter sp. D2 have been deposited in the National Center for Biotechnology Information (NCBI) Genome database under accession number JACDXZ000000000. All the RNA-seq read data have been deposited in NCBI's sequence read archive (SRA) under project accession number PRJNA646786. The structure of DddX/ATP complex has been deposited in the PDB under the accession code 7CM9.

The following data sets were generated
    1. Wang X
    (2020) RNA-Seq of Psychrobacter sp. D2
    NCBI's sequence read archive (SRA),PRJNA646786.

Article and author information

Author details

  1. Chun-Yang Li

    College of Marine Life Sciences, Ocean University of China, Qingdao, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Xiu-Juan Wang

    State Key Lab of Microbial Technology, Marine Biotechnology Research Center, Shandong University, Qingdao, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Xiu-Lan Chen

    State Key Lab of Microbial Technology, Marine Biotechnology Research Center, Shandong University, Qingdao, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Qi Sheng

    State Key Lab of Microbial Technology, Marine Biotechnology Research Center, Shandong University, Qingdao, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Shan Zhang

    State Key Lab of Microbial Technology, Marine Biotechnology Research Center, Shandong University, Qingdao, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Peng Wang

    College of Marine Life Sciences, Ocean University of China, Qingdao, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Mussa Quareshy

    School of Life Sciences, University of Warwick, Coventry, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Branko Rihtman

    School of Life Sciences, University of Warwick, Coventry, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  9. Xuan Shao

    State Key Lab of Microbial Technology, Marine Biotechnology Research Center, Shandong University, Qingdao, China
    Competing interests
    The authors declare that no competing interests exist.
  10. Chao Gao

    State Key Lab of Microbial Technology, Marine Biotechnology Research Center, Shandong University, Qingdao, China
    Competing interests
    The authors declare that no competing interests exist.
  11. Fuchuan Li

    National Glycoengineering Research Center, Shandong University, Qingdao, China
    Competing interests
    The authors declare that no competing interests exist.
  12. Shengying Li

    National Glycoengineering Research Center, Shandong University, Qingdao, China
    Competing interests
    The authors declare that no competing interests exist.
  13. Weipeng Zhang

    College of Marine Life Sciences, Ocean University of China, Qingdao, China
    Competing interests
    The authors declare that no competing interests exist.
  14. Xiao-Hua Zhang

    College of Marine Life Sciences, Ocean University of China, Qingdao, China
    Competing interests
    The authors declare that no competing interests exist.
  15. Gui-Peng Yang

    Key Laboratory of Marine Chemistry Theory and Technology, Ocean University of China, Qingdao, China
    Competing interests
    The authors declare that no competing interests exist.
  16. Jonathan D Todd

    School of Biological Sciences, University of East Anglia, Norwich, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  17. Yin Chen

    School of Life Sciences, University of Warwick, Coventry, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0367-4276
  18. Yu-Zhong Zhang

    College of Marine Life Sciences, Ocean University of China, Qingdao, China
    For correspondence
    zhangyz@sdu.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2017-1005

Funding

National Key Research and Development Program of China (2018YFC1406700)

  • Yu-Zhong Zhang

National Science Foundation of China (91851205)

  • Yu-Zhong Zhang

National Science Foundation of China (31630012)

  • Yu-Zhong Zhang

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2021, Li et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Download links

Share this article

https://doi.org/10.7554/eLife.64045

Further reading

    1. Ecology
    2. Evolutionary Biology
    Vendula Bohlen Šlechtová, Tomáš Dvořák ... Joerg Bohlen
    Research Article

    Eurasia has undergone substantial tectonic, geological, and climatic changes throughout the Cenozoic, primarily associated with tectonic plate collisions and a global cooling trend. The evolution of present-day biodiversity unfolded in this dynamic environment, characterised by intricate interactions of abiotic factors. However, comprehensive, large-scale reconstructions illustrating the extent of these influences are lacking. We reconstructed the evolutionary history of the freshwater fish family Nemacheilidae across Eurasia and spanning most of the Cenozoic on the base of 471 specimens representing 279 species and 37 genera plus outgroup samples. Molecular phylogeny using six genes uncovered six major clades within the family, along with numerous unresolved taxonomic issues. Dating of cladogenetic events and ancestral range estimation traced the origin of Nemacheilidae to Indochina around 48 mya. Subsequently, one branch of Nemacheilidae colonised eastern, central, and northern Asia, as well as Europe, while another branch expanded into the Burmese region, the Indian subcontinent, the Near East, and northeast Africa. These expansions were facilitated by tectonic connections, favourable climatic conditions, and orogenic processes. Conversely, aridification emerged as the primary cause of extinction events. Our study marks the first comprehensive reconstruction of the evolution of Eurasian freshwater biodiversity on a continental scale and across deep geological time.

    1. Ecology
    2. Neuroscience
    Kathleen T Quach, Gillian A Hughes, Sreekanth H Chalasani
    Research Article

    Prey must balance predator avoidance with feeding, a central dilemma in prey refuge theory. Additionally, prey must assess predatory imminence—how close threats are in space and time. Predatory imminence theory classifies defensive behaviors into three defense modes: pre-encounter, post-encounter, and circa-strike, corresponding to increasing levels of threat—–suspecting, detecting, and contacting a predator. Although predatory risk often varies in spatial distribution and imminence, how these factors intersect to influence defensive behaviors is poorly understood. Integrating these factors into a naturalistic environment enables comprehensive analysis of multiple defense modes in consistent conditions. Here, we combine prey refuge and predatory imminence theories to develop a model system of nematode defensive behaviors, with Caenorhabditis elegans as prey and Pristionchus pacificus as predator. In a foraging environment comprised of a food-rich, high-risk patch and a food-poor, low-risk refuge, C. elegans innately exhibits circa-strike behaviors. With experience, it learns post- and pre-encounter behaviors that proactively anticipate threats. These defense modes intensify with predator lethality, with only life-threatening predators capable of eliciting all three modes. SEB-3 receptors and NLP-49 peptides, key stress regulators, vary in their impact and interdependence across defense modes. Overall, our model system reveals fine-grained insights into how stress-related signaling regulates defensive behaviors.